Comparative analysis of the male reproductive accessory glands of bat species from the five Brazilian Subfamilies of the family Phyllostomidae (Chiroptera)

This study aimed to morphologically characterize and compare the male reproductive accessory glands (RAGs) of bats belonging to the five Brazilian subfamilies of the family Phyllostomidae (Carollia perspicillata—Carollinae; Desmodus rotundus—Desmodontinae; Glossophaga soricina—Glossophaginae; Phyllostomus discolor—Phyllostominae and Platyrrhinus lineatus—Stenodermatinae). The study demonstrated that the RAGs of phyllostomid bats were comprised of a pair of extra‐abdominal bulbourethral glands and an intra‐abdominal complex, composed of paraurethral glands and a prostate with two (Desmodontinae and Stenodermatinae) or three (Carollinae, Glossophaginae and Phyllostominae) different regions, with the absence of the seminal vesicles; this pattern possibly evolved from a process of compaction of the prostatic regions from an ancestor with three regions. J. Morphol. 276:470–480, 2015. © 2014 Wiley Periodicals, Inc.     

Morphological analysis of the male reproductive accessory glands of the bat Artibeus lituratus (Phyllostomidae: Chiroptera)

Bats are distributed worldwide from tropical to temperate regions. Despite their wide geographical radiation and advances in studies using evolutionary approaches, aspects related to the reproduction of these animals remain poorly explored, especially those related to the male reproductive accessory glands (RAGs). Thus, the aim of this study was to analyze the morphophysiology of the male RAGs in the bat Artibeus lituratus. The RAGs in A. lituratus are composed of a compact intra‐abdominal glandular complex, consisting of the prostate with two prostatic regions (ventral and dorsal), plus Littre glands and a pair of extra‐abdominal bulbourethral glands. The ventral region of the prostate has an epithelium with variable morphology, due to its holocrine type of secretion. In contrast, the dorsal region has a typical cubic‐to‐columnar pseudostratified epithelium. Both regions contain two cell types, basal and secretory cells. Similar to the epithelial morphology, the secretion also varies, with the ventral region containing numerous PAS‐positive globular vesicles, whereas the dorsal region has a more fluid, hyaline and PAS‐negative secretion. Littre glands are dispersed in the connective tissue of the urethra, while the bulbourethral glands are located in the penile root, both glands with cubic‐to‐columnar pseudostratified epithelium and globular PAS‐positive secretion. The results demonstrate that the RAGs of A. lituratus are composed of two prostatic regions, ventral and dorsal, and urethral and bulbourethral glands, with no seminal vesicles. Each prostatic region has unique and distinctive characteristics, with the ventral region presenting an exclusive holocrine nature and the dorsal region having similarities to the ventral prostate of rodents.     

Postnatal cranial ontogeny of the Greater Bulldog Bat Noctilio leporinus (Chiroptera: Noctilionidae)

We studied the postnatal development of the skull of Noctilio leporinus, examining the relationship between ectocranial elements, including shape changes and sutures closure and fusion. Most shape changes and structure development were observed at subadults and adults; zygomatic arch, sagittal crest, occipital process and mandibular processes developed noticeably up to the adult stage. Cranial sutures closure and fusion sequences of N. leporinus agree with that of hystricomorph rodents, artiodactyls, primates, sirenians and carnivores, beginning with the cranial vault followed by the basicranium, supporting a conserved pattern for mammalia. Detailed comparisons exhibit a complete cranial sutures fusion reached earlier at Desmodus rotundus regarding N. leporinus and Pteropus sp., and an early fusion for the sutura coronalis plus late fusion for the sutura sagittalis at N. leporinus regarding Desmodus rotundus. The drastic shape changes of cranial elements, as well as sutures closure and fusion in N. leporinus at subadults and adults, seem to be closely related to the acquisition of morphological specializations during stages of development when the fisher bat begins to feed independently.     

Ultrastructure of male accessory glands of Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae)

The ultrastructure of the male accessory glands of the blow fly, Chrysomya megacephala (Fabricius), was presented using light microscopy (LM), scanning electron microscopy (SEM), and transmission electron microscopy (TEM). A pair of accessory glands was separated at opposite sites. Morphometric results using LM yield evidenced no significant difference in the median of either length or width of the left and right glands. A significant increment in both length and width was seen to plateau between three to six days. SEM observation showed that the surface of the glands revealed a faint irregular groove pattern throughout, and it was occasionally penetrated by tracheoles. Each gland was a slender, elongated sac‐like tubule having apical rounded ends, with a slight constriction at the sub‐apical part of the gland being observed occasionally. TEM analyses of three‐day‐old males showed that the glands consisted of external capsular cells with a basement membrane underneath, glandular cells, and gland lumen. The capsular cell was flat and contained a nucleus with electron dense material in the nuclear envelope. The glandular cell, appearing as columnar, consisted of a vacuolated component that contained a large oval nucleus centrally or sub‐basally located, with dense mitochondria, numerous rough endoplasmic reticulum, and secretory vesicles containing electron‐lucent materials. In the gland lumen, the cross‐section through the middle portion revealed dense secretory materials, characterized by electron‐dense materials. Some sections revealed a large lumen where secretion accumulates within the delicate sac. The seven‐day‐old glands exhibited a remarkable change in the lumen, where the whole space contained a large amount of secretory materials, with the electron‐dense materials being characterized as similar to those observed in three‐day‐old glands. About four prominent types of secretions were observed on the basis of difference in electron‐density.     

Comparative hindlimb bone morphology in noctilionid fisher bats (Chiroptera: Noctilionidae), with emphasis on Noctilio leporinus postnatal development

The hindlimbs allow bats to attach to the mother from birth, and roost during independent life. Despite the great morphological diversity in Chiroptera, the hindlimbs morphology and its postnatal development have been poorly studied. Postnatal development of hindlimbs in Noctilio leporinus is described, further comparing the morphology of adults with that of Noctilio albiventris and previously reported species (Desmodus rotundus, Artibeus lituratus, Molossus molossus). The ossification ending sequence at autopodium elements of N. leporinus does not follow the distal to proximal directional sequence described for D. rotundus, exhibiting a heterochronic delayed ossification ending for the digits of N. leporinus regarding other hindlimb elements, associated with the bigger relative autopodium size of this fisher bat regarding other bat species. Noctilionid bats share the same adult hindlimb bone morphology, except for differences at hindlimb proportions and calcar ossification degree. There are differences in the number and position of bony processes, slots and sesamoids of adult noctilionid fisher bats regarding previously reported species; most differences are concentrated at the autopodium and are related to an increased surface for muscular insertion and the structural support of claws. These facts seem to be closely associated with functional demands of the feeding strategy of noctilionid fisher bats.     

Nuclear binding sites for juvenile hormone III in the male accessory reproductive glands of Melanoplus sanguinipes

Summary

We have identified a potential nuclear juvenile hormone (JH) receptor in the long hyaline tubules (LHT), part of the male accessory reproductive gland (MARG) of M. sanguinipes. The MARG was incubated in vitro with [³H]JH III, and the distribution of the [³H]JH III among the cellular fractions of the LHT was determined. Some 37±4% of the radioactivity was associated with the crude nuclear pellet, while the cytosolic, microsomal and mitochondrial fractions contained 30±3%, 23±2% and 10±1%, respectively. The bound JH III was measured in nuclear extracts of LHT from males up to 15 days post-eclosion. These results revealed that JH binding increased in an age-dependent manner up to day 7, then levelled off to day 12, to increase again on day 14. The nuclear-binding component in the LHT had a very strong affinity for JH III, with a K_D value of 0.8 nM. Our observations are considered in relation to the potential site and mode of action of JH.     

Evidences of the extraglandular origin of two secretory proteins in the male accessory reproductive glands of Chilo partellus (Pyralidae,Lepidoptera, Insecta)

Summary

The male accessory reproductive glands (MARG) play an important role in contributing proteins for the formation of the spermatophore, a structure that transports sperm from the male to the female. Several studies have shown that these proteins could be either of intraglandular or extraglandular origin. SDS-PAGE analysis revealed proteins in the adult MARG of Chilo partellus, which comigrate with the larval hemolymph proteins (LHP). Ouchterlony's immunodiffusion showed that the antiserum raised against MARG extract cross-reacts with the proteins present in the adult hemolymph and fat body. Immunoprecipitates of labelled hemolymph proteins with anti-LHP or anti-MARG proteins reveal two polypeptides that comigrate with LHPs. Thus, there appear to be some proteins of extraglandular origin in the MARG of C. partellus, and the LHP could belong to this category.     

Histology and histochemistry of the accessory reproductive glands in the male hairy-nosed wombat (Lasiorhinus latifrons)

The accessory male reproductive glands of the hairy-nosed wombat, Lasiorhinus latifrons, are a prostate and three pairs of Cowper's glands. Component units of all are branched tubular structures of varying epithelial makeup and secretory content. The prostate has the carrotlike shape and three consecutive regions commonly found in marsupials. The regions differ in their tubular histology and histochemistry: all contain secretory globules in glandular lumina. Cowper's glands A and B are histologically identical except for the absence of interstitial mast cells from gland G: gland C is characterized by narrower tubules and larger epithelial cells. Histochemical tests for protein, carbohydrate and iron indicate that glycogen is a major secretory product of the prostate (largely posterior region), iron is also secreted (mainly posterior region) and a small quantity of acid mucin is produced (mainly central region). Glycogen is a feature also of anterior prostatic glandular epithelium and of the capping cells of the urethral transitional epithelium. Cowper's gland A has considerable protein in its secretion, gland B a neutral glycoprotein and gland C a sialomucin: the latter two also exhibit cytoplasmic glycogen in their secretory cells.     

Observations on the production of purple pigments in the egg capsules,hypobranchial and reproductive glands from seven species of Muricidae (Gastropoda: Mollusca)

Summary

Tyrian purple is a well-known colourant that can be obtained from the hypobranchial glands of muricids. Here we investigate the presence of purple and related pigments in the hypobranchial glands, reproductive glands and egg capsules of three Rapaninae, three Ocenebrinae and one Muricinae species. Observations on the dissected specimens revealed the presence of purple pigmentation in the hypobranchial glands of all species. All of the Rapaninae and the Muricinae, but only some species of Ocenebrinae, appear to transfer the pigment precursors to their egg capsules. This provides evidence that the precursors of Tyrian purple are not produced for the sole purpose of protecting the egg masses as has been previously suggested. In all the subfamilies, the hypobranchial and reproductive (capsule and prostate) glands lie adjacent to one another. Colour changes in the reproductive glands, indicating the presence of dye precursors, were observed in two species of Rapaninae. In Dicathais orbita, colour changes could be seen in both the capsule glands of females and prostrate glands of males. The final colour was more red in the reproductive glands than the purple observed in the hypobranchial glands. Preliminary observations of detached hypobranchial gland sections in both D. orbita and Pterynotus triformis indicate a different suite of colour reactions occur when compared to sections that are intact and attached to the reproductive glands. This demonstrates that the reproductive glands can influence the chemical conversions of dye precursors synthesized by these species. Further studies on the secondary metabolism occurring within the hypobranchial glands and reproductive organs of Muricidae are ongoing, including histological sectioning and confirmation of the chemistry behind the colours observed and functional analysis of Tyrian purple precursors.     

Histology and histochemistry of the accessory reproductive glands in the male hairy-nosed wombat (Lasiorhinus latifrons)

Summary The accessory male reproductive glands of the hairy-nosed wombat, Lasiorhinus latifrons, are a prostate and three pairs of Cowper's glands. Component units of all are branched tubular structures of varying epithelial makeup and secretory content. The prostate has the carrotlike shape and three consecutive regions commonly found in marsupials. The regions differ in their tubular histology and histochemistry: all contain secretory globules in glandular lumina. Cowper's glands A and B are histologically identical except for the absence of interstitial mast cells from gland B: gland C is characterized by narrower tubules and larger epithelial cells. Histochemical tests for protein, carbohydrate and iron indicate that glycogen is a major secretory product of the prostate (largely posterior region), iron is also secreted (mainly posterior region) and a small quantity of acid mucin is produced (mainly central region). Glycogen is a feature also of anterior prostatic glandular epithelium and of the capping cells of the urethral transitional epithelium. Cowper's gland A has considerable protein in its secretion, gland B a neutral glycoprotein and gland C a sialomucin: the latter two also exhibit cytoplasmic glycogen in their secretory cells.     

The ultrastructure of the male accessory reproductive glands of the colorado beetle

Summary The accessory reproductive glands of Leptinotarsa decemlineata males are simple epithelial tubular glands. They are surrounded by a network of slow acting muscle cells. All the gland cells have a very extensive granular endoplasmic reticulum, a prominent Golgi apparatus, but few secretory granules. The secretory product in the lumen, which is a neutral mucopolysaccharide-protein complex, appears as a granular material in which fibrillar structures occur. Neither in the gland cells nor in the lumen were regional differences observed. After allatectomy the gland cells degenerate in a remarkable way. A zone containing microvillous structures appears between the outer and inner cells. While the inner cells degenerate completely, the outer ones do not but become organised for minimal consumption of energy, necessary to survive diapause.Grateful acknowledgment is made for a mandate as Aangesteld Navorser of the National Foundation of Scientific Research in Belgium.We wish to thank Ing. W. Bohijn for operating the EM and Mr. G. Maes for photography.     

Male reproductive tract and accessory glands of a stomatopod,Squilla holoschista

In S. holoschista, the vas deferens is differentiated into 3 regions based on the functional morphology of the epithelial lining. The proximal part with a highly secretory epithelial layer may be responsible for the secretion which is rich in protein, and moderately so in carbohydrate and lipid substances. The mid-region serves for storage of the spermatozoa. The distal part has specialized epithelial cells of a secretory nature. In addition, there are 4 typhlosole-like ridges fringed with cilia which probably aid in the conduction of the sperm cord during copulation. Secretions of the accessory reproductive glands contain a large number of discrete granules rich in mucoprotein. The principal function of this secretion appears to be the digestion of the sperm cord in the oviduct.     

Gene expression changes in male accessory glands during ageing are accompanied by reproductive decline in Drosophila melanogaster

Senescence is accompanied by loss of reproductive functions. Here, we studied reproductive ageing in Drosophila melanogaster males and asked whether the expected decline in male reproductive success is due to diminished functionality of the male accessory gland (AG). The male AG produces the majority of seminal fluid proteins (SFPs) transferred to the female at mating. SFPs induce female postmating changes and are key to male reproductive success. We measured age‐dependent gene expression changes for five representative SFP genes in males from four different age groups ranging from 1 to 6 weeks after eclosion. Simultaneously, we also measured male reproductive success in postmating traits mediated by transfer of these five SFPs. We found a decreased in male SFP gene expression with advancing age and an accompanying decline in male postmating success. Hence, male reproductive senescence is associated with a decline in functionality of the male AG. While overall individual SFP genes decreased in expression, our results point towards the idea that the composition of an ejaculate might change with male age as the rate of change was variable for those five genes.     

Induction of the acrosome reaction in the spermatozoa of the goat by secretions of the male accessory glands and milk

The balancing effects of bulbourethral gland secretion (BUS) and of seminal vesicle secretion (SVS) on goat semen quality were previously demonstrated. In the present study, electron microscope observations revealed a high frequency of spermatozoa with a reacted acrosome among spermatozoa from cauda epididymis exposed to BUS in the presence of milk. This frequency was significantly reduced when SVS had been added either before or after BUS. No reacted acrosome was observed in the absence of milk. All mount spermatozoa were incubated with milk or SVS or BUS or combinations of the three materials labeled with colloidal gold. SVS attached specifically on the plasma membrane covering the anterior part of the acrosome, whereas BUS spread all over the sperm head. Milk attached on the anterior half of the sperm head only when BUS was present in the sperm environment. It is concluded that BUS plays an active role in the induction of the acrosome reaction in the presence of milk and that SVS counteracts this role.     

The reproductive cycle of male tomb bats, Taphozous hildegardeae (Chiroptera: Emballonuridae), in a seasonal environment of the African tropics

Two cave populations of Hildegarde's tomb bat had a reproductive cycle that corresponded closely to the rainfall-induced seasonality of coastal Kenya (4s). Males had pronounced bimodal cycles of body weight due to the deposition of fat during periods of relative food abundance in both rainy seasons, and fat depletion during competitive mating and the dry seasons, when numbers of moths were lowest. The main period of sexual regeneration coincided with the increase in body weight experienced during the 'long rains' [April-June) and led to mating. A secondary peak in the weights of male sexual glands, associated with the increase in body weight that occurred in the 'short rains' (October-December), did not result in reproduction. It is suggested that this latter period of sexual activity was related to the maintenance of year-round harems, and may represent the male response to a vestigial, bimodally polyoestrous, reproductive cycle.     

Comparative morphology of male reproductive systems in Mediterranean blennies (Blenniidae)

The male reproductive organs of 16 species of Mediterranean Blenniidae ( Aidablennius sphynx, Blennius ocellaris, Coryphoblennius galerita, Lipophrys adriaticus, L. canevae, L. dalmatinus, L. nigriceps, Parablennius gattorugine, P. incognitus, P. sanguinolentus, P. rouxi, P. tentacularis, P. zvonimiri, Paralipophrys trigloides, Salaria pavo and Scartella cristata ) consist of pairs of testes, testicular glands, spermatic ducts, and blind pouches. Three main types of accessory sex organs were found by comparing the external morphology of the male gonads. Differences between species were observed in the volume of the testicular gland in relation to the volume of the testis and in the size and length of the spermatic ducts, and blind pouches. The anatomy of the testicular glands of all species investigated do not differ. Each gland consists of ducts that appear to be tubules which terminate at the testis periphery on one side and at the spermatic duct on the other side. Contrary to previous claims, A. sphynx has no fat body in place of the testicular gland; the gland of this species was not distinguishable from that of the other species investigated. In the Lipophrys species, in P. trigloides , and in B. ocellaris , a transition zone between testis and testicular gland is present. The testicular blind pouches empty into the spermatic ducts, into the ureter, or separately on the genital papilla. In most species, the epithelium has no or low folds, while in S. pavo it possesses high folds that nearly fill the lumen of the blind pouches. The morphological results are discussed in connection with taxonomy, ecology, and behaviour of the fishes.     

Social Organization and Foraging Behaviour of the Fishing Bat,Noctilio leporinus (Chiroptera:Noctilionidae)

Female Noctilio leporinus roost in groups that remain together, associated with the same individuals and in the same location, for several years regardless of turnover in resident males and movements of the group to alternate roosts. Females scent marked themselves with the sub-axial secretions of other females by rubbing their heads beneath other bats' wings. Males residing with female groups retain their tenure for two or more reproductive seasons. Bachelor males roost solitarily or in small groups apart from females. Together, these characteristics appear to form the basis of a polygynous social organization. Female N. leporinus foraged solitarily or in small groups with other females from the same roost group. Stable female roost groups forage together and return to the same foraging areas over long periods of time. Bats assembled into small groups outside of the roost and flew together to foraging areas. Females from one roost group were monitored using the same foraging area for over a year. Bats foraged close enough to each other to communicate the location of prey either passively or actively. Roosts were not used as information centres, as bats rarely followed each other from the roost to forage. Males foraged solitarily, utilizing areas that were different from, and larger than, those of the females.     

Structure of the accessory reproductive glands of the male migratory grasshopper,Melanoplus sanguinipes

The accessory reproductive glands of Melanoplus sanguinipes comprise two bilateral masses of 16 tubules each, distinguishable in sexually mature insects as four white, ten short hyaline, one long hyaline, and a seminal vesicle. Over most of its length, the wall of each tubule consists of a simple glandular epithelium resting on a basal lamina, surrounded by a thin layer of circular muscle. However, near the junction with the ejaculatory duct, the wall of each tubule has a much thickened circular muscle layer and squamous or cuboidal epithelium, the region serving to regulate movement of secretion into the ejaculatory duct. Interdigitation of adjacent epithelial cells is common, and several kinds of specialized junctions occur. In the glandular region, all epithelial cells appear the same and may be flattened, cuboidal, or columnar depending on the tubule type. Except for those of the seminal vesicle, the glandular epithelial cells share ultrastructural features typical of cells engaged in the synthesis of protein for export. Despite these general similarities, in most instances subtle differences occur in the cellular ultrastructure of the epithelia of each tubule and in the appearance of their luminal secretions, suggesting that the tubules are functionally specialized.     

Ultrastructure of the male accessory ducts and prostate gland of Diclidophora merlangi (Monogenoidea)

The vas deferens, seminal vesicle, penis and common genital atrium of the monogenean, Diclidophora merlangi are lined by a very flat, lamellate epithelium. The structure is apparently syncytical, although nuclei or perikaryons have not been observed. The epithelium extends to just inside the gonopore where a septate desmosome marks the union with body tegument. There is minor regional variation in structure. The terminal portion of the seminal vesicle and the penis lumen are lined in part by the luminal cytoplasm of the prostate gland which surrounds this part of the reproductive tract. The prostate gland cells are synthetically active and produce a characteristic secretory body that is released either singly by exocytosis, involving membrane fusion, or in bulk via apocrine secretion. The secretion is acidophilic, PAS-positive and reactive for protein. The penis is sucker-like in structure and armed with a ring of 16 genital hooklets. Cilia have not been observed in any part of the male reproductive tract, and sense receptors are not apparent in the tegument surrounding the gonopore.